The party supported the Prodi I Cabinet until 1998, when Bertinotti's Communists turned to opposition and the government lost its majority in Parliament. However this decision was divisive also in Bertinotti's camp, where a group of dissidents, led by President of the party Armando Cossutta, split off and founded a rival communist outfit, the Party of Italian Communists (PdCI), which joined Massimo D'Alema's first cabinet.

In October 2004, the PRC joined the centre-left opposition and in April 2005, Nichi Vendola, an openly gay politician and one of the emerging leaders of the party, was elected President of traditionally conservative Apulia Region, due to the support of the whole centre-left and after a primary election, which saw Vendola beat a centrist opponent. He was the only regional President ever belonging to the PRC.

The decision to participate in the centre-left coalition government, and in particular the party's decision to vote to refinance the Italian military presence in Afghanistan and send troops to Lebanon attracted criticism from other sections of the European far left[2] and provoked the splits of many groups, notably the Communist Workers' Party, the Communist Alternative Party and Critical Left.

In April 2008, following the severe defeat of the party in the 2008 general election, a group of former Bertinottiani, composed primarily of former members of Proletarian Democracy, led by Paolo Ferrero and Giovanni Russo Spena, allied with other minority factions to force secretary Franco Giordano to resign. They criticised The Left – The Rainbow alliance and the political line of Fausto Bertinotti.

In the July congress the internal left-wing prevailed over Bertinottiani and Paolo Ferrero was elected new secretary. He was supported by a bare majority 53% of the party delegates, and the party remained divided around factional and regional lines with Vendola, the standard-bearer of Bertinottiani, accusing Northern delegates of having absorbed leghismo and stating that "it was the end of the party I knew".[3]

In the 2013 general election the PRC was part of the Civil Revolution coalition, which obtained 2.2% of the vote and no seats.[12] Disappointed by this result, the party's central committee scheduled an "extraordinary conference" to be held later in 2013, which would radically re-envision the party's program, objectives, and methods.[13] In particular, the party's central committee reprimanded itself for "... a top down method of unity [...] treaty agreements between elites, which only caused further division and fragmentations." The party's regional secretaries gathered in April to organize the event.[13]

In February 2007 Senator Franco Turigliatto, one of the leaders of Critical Left along with Salvatore Cannavò, voted against two motions on the government's foreign policy, leading Romano Prodi to temporarily resign as Prime Minister. In April Turigliatto was expelled from the party and thus Critical Left was suspended from it. In December the group officially left PRC to be transformed into a party.

At that point Being Communists suffered a split by those who opposed the decision of leader Claudio Grassi to vote in favour of the expulsion of Senator Turigliatto from the party: a group, led by Fosco Giannini, left the faction and launched The Ernesto, without leaving the party itself.

In the 24–27 July 2008 congress the Refoundation in Movement motion of Ferrero and Grassi (40.1%) faced the bulk of Bertinottiani, who organized themselves around the motion titled Manifesto for the Refoundation (47.6%) with Nichi Vendola as standard-bearer. The Ernesto of Giannini and Counter-current (7.7%), HammerSickle of Claudio Bellotti (3.2%) and a minor group of former Bertinottiani called "Disarm, Renew, Refound" (1.5%) decided to join forces with the Ferrero-Grassi group. Vendola, defeated by Ferrero, announced the creation of a new minority faction, Refoundation for the Left (RpS).[3][14]